Skip to main content

Alterations of Synaptic Ultrastructure Induced by Hippocampal Kindling

  • Chapter
Kindling 4

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 37))

Abstract

Kindling, first discovered by the late Graham Goddard1, is widely regarded as a dramatic, reliable and robust form of neural plasticity2–6. One of the most remarkable features of kindling is that it induces a virtually permanent change in brain function. Synaptic responsiveness of the circuit stimulated during kindling undergoes an augmentation which persists, without further reinforcement, for many months5–9. This exceptionally enduring enhancement of synaptic efficacy caused by kindling and the dependence of the process on protein synthesis10,11 and axonal transport12,13 imply an underlying structural modification of the synapse itself.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. G. V. Goddard, Development of epileptic seizures through brain stimulation of low intensity, Nature 214: 1020 (1967).

    Article  PubMed  CAS  Google Scholar 

  2. G. V. Goddard and R. M. Douglas, Does the engram of kindling model the engram of normal long term memory?, Can. J. Neurol. Sci. 2: 385 (1975).

    PubMed  CAS  Google Scholar 

  3. R. Racine, L. Tuff, and J. Zaide, Kindling, unit discharge and neural plasticity, Can. J. Neurol. Sci. 2: 395 (1975).

    PubMed  CAS  Google Scholar 

  4. R. Racine, Kindling: the first decade, Neurosurgery 3: 234 (1978).

    Article  PubMed  CAS  Google Scholar 

  5. G. V. Goddard, The kindling model of epilepsy, Trends Neurosci. 6: 275 (1983).

    Article  Google Scholar 

  6. F. Morrell and L. deToledo-Morrell, Kindling as a model of neuronal plasticity, in: “Kindling 3”, J. A. Wada, ed., Raven, New York (1986).

    Google Scholar 

  7. G. V. Goddard, D. C. McIntyre, and C. K. Leech, A permanent change in brain function resulting from daily electrical stimulation, Exp. Neurol. 25: 295 (1969).

    Article  PubMed  CAS  Google Scholar 

  8. J. A. Wada and M. Sato, Generalized convulsive seizures induced by daily electrical stimulation of the amygdala in cats: correlative electrgraphic and behavioral seizures, Neurology (Minneap.) 24: 565 (1974).

    CAS  Google Scholar 

  9. F. Morrell, Goddard’s kindling phenomenon, in: “Chemical Modulation of Brain Function”, H. C. Sabelli, ed., Raven, New York (1973).

    Google Scholar 

  10. F. Morrell, N. Tsuru, T. J. Hoeppner, D. Morgan, and W. H. Harrison, Secondary epileptogenesis in frog forebrain: effect of inhibition of protein synthesis, Can. J. Neurol. Sci. 2: 407 (1975).

    PubMed  CAS  Google Scholar 

  11. V. Jonec and C. G. Wasterlain, Effects of inhibitors of protein synthesis on the development of kindled seizures in rats, Exp. Neurol. 66: 524 (1979).

    Article  PubMed  CAS  Google Scholar 

  12. F. Morrell, Biochemical alterations in secondary epileptogenic lesions, in: “Secondary Epileptogenesis”, A. Mayersdorf and R. P. Schmidt, eds., Raven, New York (1982).

    Google Scholar 

  13. F. Morrell, Callosal mechanisms in epileptogenesis, in: “Epilepsy and the Corpus Callosum”, A. Reeves, ed., Plenum, New York (1985).

    Google Scholar 

  14. R. Racine and J. Zaide, A further investigation into the mechanisms underlying the kindling phenomenon, in: “Limbic Mechanisms”, K. L. Livingston and O. Hornykiewicz, eds., Plenum, New York (1978).

    Google Scholar 

  15. M. Langmeier and J. Mares, Changes in some ultrastructural parameters of cortical synapses in the initial phases of kindling, Physiol. Bohemoslov. 33: 367 (1984).

    PubMed  CAS  Google Scholar 

  16. A. J. Cronin, T. P. Sutula, and N. L. Desmond, Morphological changes in the hippocampal dentate gyrus accompany kindling of the entorhinal cortex, Soc. Neurosci. Abstr. 13: 947 (1987).

    Google Scholar 

  17. N. Hawrylak, F.-L. Chang, D. Treacy, K. R. Isaaks, and W. T. Greenough, Synaptogenesis in kindling, Soc. Neurosci. Abstr. 14: 881 (1988).

    Google Scholar 

  18. T. Sutula, H. Xiao-Xian, J. Cavazos and G. Scott, Synaptic reorganization in the hippocampus induced by abnormal functional activity, Science 239: 1147 (1988).

    Article  PubMed  CAS  Google Scholar 

  19. H. J. G. Gundersen, Stereology of arbitrary particles, J. Microsc. 143: 3 (1986).

    Article  PubMed  CAS  Google Scholar 

  20. H. Brændgaard and H. J. G. Gundersen, The impact of recent stereological advances on quantitative studies of the nervous system, J. Neurosci. Meth. 18: 39 (1986).

    Article  Google Scholar 

  21. C. A. Curcio and J. W. Hinds, Stability of synaptic density and spine volume in dentate gyrus of aged rats, Neurobiol. Aging 4: 77 (1983).

    Article  PubMed  CAS  Google Scholar 

  22. D. C. Sterio, The unbiased estimation of number and sizes of arbitrary particles using the disector, J. Microsc. 134: 127 (1984).

    Article  PubMed  CAS  Google Scholar 

  23. Y. Geinisman, F. Morrell, and L. deToledo-Morrell, Remodeling of synaptic architecture during hippocampal kindling, Proc. Natl. Acad. Sci. U.S.A. 85: 3260 (1988).

    Article  CAS  Google Scholar 

  24. A. Hjorth-Simonsen, Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata, J. Comp. Neurol. 146: 219 (1972).

    Article  PubMed  CAS  Google Scholar 

  25. A. Hjorth-Simonsen and B. Jeune, Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation, J. Comp. Neurol. 144: 215 (1972).

    Article  PubMed  CAS  Google Scholar 

  26. O. Steward, Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat, J. Comp. Neurol. 167: 285 (1976).

    Article  PubMed  CAS  Google Scholar 

  27. D. L. Rosene and G. W. Van Hoesen, The hippocampal formation of the primate brain, in: “Cerebral Cortex”, Vol. 6, E. G. Jones and A. Peters, eds., Plenum, New York (1987).

    Google Scholar 

  28. M. Nieto-Sampedro, S. F. Hoff, and C. W. Cotman, Perforated postsynaptic densities: probable intermediates in synapse turnover, Proc. Natl. Acad. Sci. U.S.A. 79: 5718 (1982).

    Article  PubMed  CAS  Google Scholar 

  29. Y. Y. Geinisman, V. N. Larina, and V. N. Mats, Changes of neurones dimensions as a possible morphological correlate of their increased functional activity, Brain Res. 26: 247 (1971).

    Google Scholar 

  30. Y. Geinisman, L. deToledo-Morrell, and F. Morrell, Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory, Brain Res. 398: 266 (1986).

    Article  PubMed  CAS  Google Scholar 

  31. H. J. G. Gundersen, Notes on the estimation of the numerical density of arbitrary profiles: the edge effect, J. Microsc. 111: 219 (1987).

    Article  Google Scholar 

  32. D. A. Matthews, C. Cotman, and G. Lynch, An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration, Brain Res. 115: 1 (1986).

    Article  Google Scholar 

  33. J. O. McNamara, M. Byrne, R. Danshieff, and J. Fitz, The kindling model of epilepsy: a review, Prog. Neurobiol. 15: 139 (1980).

    Article  PubMed  CAS  Google Scholar 

  34. C. E. Ribak, R. M. Bradburne, and A. B. Harris, A preferential loss of gabaergic symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex, J. Neurosci. 2: 1725 (1982).

    PubMed  CAS  Google Scholar 

  35. R. S. Sloviter, decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy, Science 235: 73 (1987).

    Article  PubMed  CAS  Google Scholar 

  36. L. P. Tuff, R. J. Racine, and R. Adamec, The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Paired pulse depression, Brain Res. 277: 79 (1983).

    Article  PubMed  CAS  Google Scholar 

  37. G. V. Goddard and E. Maru, Forces for and against the kindled state as revealed by EEG and field potential analysis in the hippocampal dentate area of perforant path kindled rats, la: “Kindling 3”, J. A. Wada, ed., Raven, New York (1986).

    Google Scholar 

  38. P. Andersen, B. Holmquist, and P. E. Voorhoeve, Entorhinal activation of dentate granule cells, Acta Physiol. Scand. 66: 448 (1966).

    Article  PubMed  CAS  Google Scholar 

  39. T. Loma, Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation, Exp. Brain Res. 12: 18 (1971).

    Google Scholar 

  40. A. Peters and I. R. Kaiserman-Abramof, The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines, Z. Zelifosch. 100: 487 (1969).

    Article  CAS  Google Scholar 

  41. A. M. Sirevaag and W. T. Greenough, Differential rearing effects on rat visual cortex synapses. II. Synaptic morphometry, Dev. Brain Res. 19: 215 (1985).

    Article  Google Scholar 

  42. S. E. Dyson and D. G. Jones, Quantitation of terminal parameters and their interrelationships in maturing central synapses: a perspective for experimental studies, Brain Res. 183: 43 (1980).

    Article  PubMed  CAS  Google Scholar 

  43. C. J. Wilson, P. M. Groves, S. T. Kitai, and J. C. Linder, Three-dimensional structure of dendritic spines in the rat neostriatum, J. Neurosci. 3: 383 (1983).

    PubMed  CAS  Google Scholar 

  44. K. M. Harris and J. K. Stevens, Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics, J. Neurosci. 8: 4455 (1988).

    PubMed  CAS  Google Scholar 

  45. Y. Geinisman, F. Morrell, and L. deToledo-Morrell, Axospinous synapses with segmented postsynaptic densities: a morphologically distinct synaptic subtype contributing to the number of profiles of “perforated” synapses visualized in random sections, Brain Res. 423: 179 (1987).

    Article  PubMed  CAS  Google Scholar 

  46. D. M. G. De Groot, Comparison of methods for the estimation of the thickness of ultrathin tissue sections, J. Microsc. 151: 23 (1988).

    Article  PubMed  Google Scholar 

  47. C. W. Cotman and P. T. Kelly, Macromolecular architecture of CNS synapses, in: “The Cell Surface and Neuronal Function”, C. W. Cotman, G. Poste, and G. L. Nocolson, eds., Elsevier, Amsterdam (1980).

    Google Scholar 

  48. P. Siekevitz, The postsynaptic density: a possible role in long-lasting effects in the central nervous system, Proc. Natl. Acad. Sci. U.S.A. 82: 3494 (1985).

    Article  PubMed  CAS  Google Scholar 

  49. A. A. Herrera, A. D. Grinnell, and B. Wolowske, Ultrastructural correlates of naturally occurring differences in transmitter release efficacy in frog motor nerve terminals, J. Neurocytol. 14: 193 (1985).

    Article  PubMed  CAS  Google Scholar 

  50. P. K. Carlin and P. Siekevitz, Plasticity in the central nervous system: do synapses divide?, Proc. Natl. Acad. Sci. U.S.A. 80: 3517 (1983).

    Article  PubMed  CAS  Google Scholar 

  51. S. E. Dyson and D. G. Jones, Synaptic remodelling during development and maturation: junction differentiation and splitting as a mechanism of modifying connectivity, Dey. Brain Res. 13: 125 (1984).

    Article  Google Scholar 

  52. T. V. P. Bliss and A. R. Gardner-Medwin, Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path, J. Physiol (Lond.) 232: 357 (1973).

    CAS  Google Scholar 

  53. T. Sutula and O. Steward, Quantitative analysis of synaptic potentiation during kindling of the perforant path, J. Neurophysiol. 56: 732 (1986).

    PubMed  CAS  Google Scholar 

  54. T. Sutula and O. Steward, Facilitation of kindling by prior induction of long-term potentiation in the perforant path, Brain Res. 420: 109 (1987).

    Article  PubMed  CAS  Google Scholar 

  55. N. L. Desmond and W. B. Levy, Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus, J. Comp. Neurol. 253: 466 (1986).

    Article  PubMed  CAS  Google Scholar 

  56. N. L. Desmond and W. B. Levy, Changes in the postsynaptic density with long-term potentiation in the dentate gyrus, J. Comp. Neurol. 253: 476 (1986).

    Article  PubMed  CAS  Google Scholar 

  57. G. Vrensen and J. Nunes Cardozo, Changes in size and shape of synaptic connections after visual training: an ultrastructural approach of synaptic plasticity, Brain Res. 218: 79 (1981).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1990 Plenum Press, New York

About this chapter

Cite this chapter

Geinisman, Y., Morrell, F., deToledo-Morrell, L. (1990). Alterations of Synaptic Ultrastructure Induced by Hippocampal Kindling. In: Wada, J.A. (eds) Kindling 4. Advances in Behavioral Biology, vol 37. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5796-4_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-5796-4_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-5798-8

  • Online ISBN: 978-1-4684-5796-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics